Abstract
The large numbers of duplicated pairs of genes in zebrafish compared to their mammalian counterparts has lead to the notion that expression of zebrafish co-orthologous pairs in some cases can together describe the expression of their mammalian counterpart. Here, we explore this notion by identification and analysis of a second zebrafish ortholog of the mammalian Kit receptor tyrosine kinase (kitb). We show that in embryos, kitb is expressed in a non-overlapping pattern to that of kita, in the anterior ventral mesoderm, Rohon-beardRohon–Beard neurons, the otic vesicle, and trigeminal ganglia. The expression pattern of kita and kitb in zebrafish together approximates that of Kit in mouse, with the exception that neither zebrafish kit gene is expressed in primordial germ cells, a site of kit expression in the mouse embryo. In addition, zebrafish kita is expressed in a site of zebrafish primitive hematopoiesis but not required for blood development, and we fail to detect kitb expression in sites of zebrafish hematopoiesis. Thus, the expression and function of zebrafish kit genes cannot be described as a simple partition of the expression and function of mouse Kit. We discuss the possibility that these unaccounted for expression domains and functions are derived from more ancestral gene duplications and partitioning instead of the relatively recent teleost teleost-specific duplication.
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References
Baker CVH, Sharpe CR, Torpey NP, Heasman J, Wylie CC (1995) A Xenopus c-kit-related receptor tyrosine kinase expressed in migrating stem cells of the lateral line system. Mech Dev 50:217–228
Barbazuk WB, Korf I, Kadavi C, Heyen J, Tate S, Wun E, Bedell JA, McPherson JD, Johnson SL (2000) The syntenic relationship of the zebrafish and human genomes. Genome Res 10:1351–1358
Bernex F, De Sepulveda P, Kress C, Elbaz C, Delouis C, Panthier JJ (1996) Spatial and temporal patterns of c-kit-expressing cells in WlacZ/+ and WlacZ/WlacZ mouse embryos. Development 122:3023–3033
Buehr M, McLaren A, Bartley A, Darling S (1993) Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev Dyn 198:182–189
Cornell RA, Eisen JS (2000) Delta signaling mediates segregation of neural crest and spinal sensory neurons from zebrafish lateral neural plate. Development 127:2873–2882
Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545
Geissler EN, Ryan MA, Housman DE (1988) The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55:185–192
Habeck H, Odenthal J, Walderich B, Maischein H, Schulte-Merker S (2002) Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr Biol 12:1405–1412
Hirata T, Kasugai T, Morii E, Hirota S, Nomura S, Fujisawa H, Kitamura Y (1995) Characterization of c-kit-positive neurons in the dorsal root ganglion of mouse. Brain Res Dev 85:201–211
Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N et al (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 21:946–957
Kao KR, Bernstein A (1995) Expression of Xkl-1, a Xenopus gene related to mammalian c-kit, in dorsal embryonic tissue. Mech Dev 50:57–69
Mackenzie MA, Jordan SA, Budd PS, Jackson IJ (1997) Activation of the receptor tyrosine kinase kit is required for the proliferation of melanoblasts in the mouse embryo. Dev Biol 192:99–107
McClintock JM, Kheirbek MA, Prince VE (2002) Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention. Development 129:2339–2354
Mellgren EM, Johnson SL (2004) A requirement for kit in embryonic zebrafish melanocyte differentiation is revealed by melanoblast delay. Genes Dev 241:493–502
Motro B, van der Kooy D, Rossant J, Reith A, Bernstein A (1991) Contiguous patterns of c-kit and steel expression: analysis of mutations at the W and Sl loci. Development 113:1207–1221
Parichy DM, Rawls JF, Pratt SJ, Whitfield TT, Johnson SL (1999) Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development 126:3425–3436
Riley BB (2003) Genes controlling the development of the zebrafish inner ear and hair cells. Curr Top Dev Biol 57:357–388
Trevarrow B, Marks DL, Kimmel CB (1990) Organization of hindbrain segments in the zebrafish embryo. Neuron 4:669–679
Acknowledgements
We thank Dr. David Parichy for aiding in the identification of kitb, and Dr. Robert Cornell for providing the zn-12 antibody. We also thank Chao Yang and Keith Hultman for useful comments on this manuscript. This work was funded by NIH grant GM56988 to S.L.J.
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Communicated by M. Hammerschmidt.
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Scheme 1
Zebrafish kitb protein sequence. This predicted full length sequence is based on our identification of exon 1 in genomic sequence, the ensembl predicted protein ENSDARP00000003199 and our own sequencing of kitb cDNA sequence (gi:58760520)
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Mellgren, E.M., Johnson, S.L. kitb, a second zebrafish ortholog of mouse Kit . Dev Genes Evol 215, 470–477 (2005). https://doi.org/10.1007/s00427-005-0001-3
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DOI: https://doi.org/10.1007/s00427-005-0001-3